Nutritional status, feeding practices and motor development of 6-month-old infants

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Nutritional status, feeding practices and

motor development of 6-month-old

infants

A.M.P Rothman

12978361

Thesis submitted for the degree Doctor Philosophiae in

Nutrition at the Potchefstroom Campus of the North-West

University

Promoter:

Dr. N.M Covic

Co-Promoters:

Prof. M Faber

Prof. C.M Smuts

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PREFACE

Acknowledgements

“Now all glory to God, Who is able, through His mighty power at work within us, to

accomplish infinitely more than we might ask or think” (Ephesians 3:20).

I wish to express my sincere gratitude and appreciation to the following people: My beloved parents,

Hettie and Thys – thank you for your endless prayers, love, support and guidance. You are my safe haven

My brothers and sisters,

Wikus, Marleen, Sarina, Martin, Michael and M.J - thank you for all your patience and making my life lighter and easier

My grandparents

Thank you for your prayers, loving kindness and wisdom My friends,

Riani, Marilize, Tammy, Lizmari, Marli, Elsabe, Nadine, Marissa, Shola, Jennifer and Karen - thank you for your prayers and sincere interests and concerns about this study

My mentors

Prof. Mieke Faber, thank you for your endless patience and determination. You have shaped the way I think as a nutritionist and I will always be grateful for the foundation you laid for me to

stand upon as a nutritionist,

Prof. Marius Smuts, thank you for trusting me to be part of the Tswaka study. Your knowledge, positive attitude and willingness to listen carried me through the study. Thank you for opening

my eyes to realise my passion for being a nutritionist.

Dr. Covic, thank you for your kind assistance as a knowledgeable study leader

Prof. Salome Kruger, prof. Grieta Hanekom and prof. Johan Jerling, thank you for the privilege to do my PhD and to be part of Centre of Excellence for Nutrition. Your confidence in me gave

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ii Colleagues

Ronel Benson and Henriëtte Claasen, thank you for your friendly administrative and logistic support. Without your assistance, this study would not be successful.

Office friends Bianca, Maryse and Alice, thank you for your encouragement and for creating a homey atmosphere in the office.

Tswaka team,

Tonderayi Matsungo - thank you for your patience and willingness to help at all times. Thank you for all team members of Tswaka. This study would not been successful if it was not for good

team work and for each and every one’s positivity and hard work. Funders,

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ABSTRACT

Background

Inadequate nutrition and development in the first thousand days have significant public health implications which include long-term effects on cognitive development and school achievement. Iron is one of the key nutrients needed for long-term growth and cognitive development. A strategy to address poor nutrition in infancy is the use of various home fortification products for example small-quantity lipid based nutritional supplements (SQ-LNS).

Aim

This study investigated the nutritional status, early feeding practices and psychomotor development of 6-month-old infants from a peri-urban community in Klerksdorp (North West Province), South Africa, as well as the acceptance of 2 novel SQ-LNS for complementary feeding by infants and their primary caregiver.

Design

The study used baseline data of a randomized controlled trial and had a cross-sectional design that included 750 6-month-old infants from a peri-urban community in the North West province in South Africa. Early feeding practices and dietary intake were investigated in association with nutritional status and psychomotor development.

For the acceptability trial, mother/infant pairs were enrolled in a two-part trial. Part 1 (n= 16) was a test-feeding trial with a cross-over, randomized design in which a five-point hedonic scale was used for sensory evaluation (disagree= 1, agree= 5). Part 2 (n= 38) was a two-week, home-use trial followed by focus group discussions.

Results

For 48.9% of the infants, exclusive breastfeeding was ceased at the age of 0–2 months. Semi-solid and/or Semi-solid foods were introduced mostly at the age of 3–4 months. At the age of 6 months, 70.1% of infants were still being breastfed. Frequently consumed complementary foods were mainly infant cereal (68.1%), formula milk (42.0%) and jarred infant foods (22.7%). Dietary intake data showed that for more than 80% of the infants, the nutrient density (amount of nutrient per 100 kcal) for iron, zinc, and calcium of the complementary diet was lower than the desired density. With regards to nutritional status, 36.4% of the infants were anaemic (Hb < 11 g/dl), 16.1% were iron deficient (plasma ferritin concentration <12 µg/l), and 9.3% of the infants suffering from iron deficiency anaemia. The anthropometric data showed that 29.3% of the infants were stunted (LAZ < 2) and 10.1% were overweight (WLZ > 2).

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Binary logistic regression analysis showed that male infants had a greater chance of being anaemic (OR= 1.388, p= 0.037). Infants who ceased being exclusively breastfed at the age of 0–2 months (OR=0.620, p=0.039) and infants who frequently consumed formula milk (OR=0.523, p=0.001) had a lower chance of being anaemic. Regarding iron deficiency (ID) status, male infants (OR=2.432, p=0.002) were found to have a greater chance to be ID; while infants with a higher birth weight (OR=0.417, p=0.005), infants who ceased being exclusively breastfed at the age of 0–2 months (OR=0.362, p=0.022), and infants who frequently consumed formula milk (OR=0.219, p=0.001), had a lower chance to be ID.

Multivariate linear regression analysis showed that haemoglobin concentration was positively related to eye-hand, locomotor and therefore also combined psychomotor activities [β= 0.677 (0.343, 1.011), p= < 0.001)]; [β= 0.439 (0.164, 0.714), p= 0.002]; [β= 1.116 (0.586, 1.645), p= < 0.001], respectively. Frequent consumption of infant cereal (≥4 days a week) was positively related to locomotor development [β= 0.709 (0.043, 1.376), p= 0.037] and parent rating scores [β= 1.506 (0.912, 2.100); p= < 0.001]. Exclusive breastfeeding up to age 0–2 months was related to higher parent rating scores [β= 1.544 (0.673, 2.414), p = 0.001)] compared to exclusive breastfeeding up to the age of 5–6 months. Male gender was associated with lower parent rating scores [β= –0.673 (–1.256, –0.089), p = 0.024], compared to female infants.

Findings from the acceptability trial showed that more than 70% of mothers reported a score of ≥4 on sensory attributes for both of the small-quantity lipid-based nutritional supplements, indicating that both supplements were well received. The mean reported consumption over the two week period was 65.3±34.2% and 62.0±31.3% of the 20 g daily portion for supplement A and B, respectively. Focus group discussions confirmed a positive attitude towards the supplements in the study population.

Conclusion

The study provides evidence that feeding practices at a very young age, including breast feeding practices, can have implications on nurtitional status and/or iron status with consequences on infant development. Associations found between feeding practices and psychomotor development may be explained by the iron status of the infants as a consequence of feeding practices. It therefore emphasises the importance of adequate iron nutrition and iron status during early infancy.

Key terms: Infant, feeding practices, nutritional status, psychomotor development, acceptability, small-quantity lipid-based nutritional supplements

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OPSOMMING

Agtergrond

Onvoldoende voeding en -ontwikkeling in die eerste duisend dae van lewe het beduidende implikasies vir die veld van openbare gesondheid en sluit ’n langtermyn-uitwerking op kognitiewe ontwikkeling en skoolprestasie in. Yster is een van die belangrikste voedingstowwe wat vir langtermyn-groei en kognitiewe ontwikkeling benodig word. Verskillende produkte word tans vir die verbetering van nutriëntinname in babas, vir gebruik voorgestel en ‘n voorbeeld hiervan is lipied-gebaseerde voedingsaanvullings

Doel

Die studie het gepoog om die voedingstatus, vroeë voedingspraktyke en motoriese ontwikkeling van 6-maande-oue babas van ’n buitestedelike Suid-Afrikaanse gemeenskap in Jouberton (Noordwes provinsie) asook die aanvaarding van twee innoverende lipied-gebaseerde voedingsaanvullings vir aanvullende voeding deur die babas en hul primêre versorgers in die studie gemeenskap, bepaal.

Studie ontwerp

Hierdie studie het 750 ses-maande-oue babas van ’n buitestedelike gemeenskap in die Noordwes-provinsie in Suid-Afrika ingesluit. Voedingspraktyke, dieëtinname en nutriëntdigtheid is in verhouding tot die voedingstatus van die babas bepaal. Verder is die assosiasie van psigomotoriese ontwikkeling met voedingspraktyke en voedingstatus vasgestel.

Vir die aanvaarbaarheidsproef, is moeder-en-baba pare vir ’n tweeledige proef ingeskryf. Deel 1 (n= 16) was ’n toets-voedingsproef met ’n oorkruis, ewekansige ontwerp waarvoor 'n vyf-punt hedoniese skaal wat vir sensoriese evaluering (verskil= 1, saamstem= 5) gebruik is. Deel 2 (n= 38) was ’n twee weeklange proef vir tuisgebruik, gevolg deur fokusgroepbesprekings.

Resultate

Vir 48,9% van die babas is uitsluitlike borsvoeding op die ouderdom van 0–2 maande gestaak. Semi-soliede en/of vaste kos is meestal op die ouderdom van 3–4 maande bygevoeg. Op die ouderdom van ses maande het 70,1% van die babas steeds borsmelk ontvang. Aanvullende voedsel-items wat gereeld ingeneem is, het hoofsaaklik babagraankos (68,1%), formule melk (42,0%) en gebottelde babavoedsel (22,7%) ingesluit. By meer as 80% van die babas was die nutriëntdigtheid (hoeveelheid van nutrient per 100 kcal) vir yster, sink en kalsium in hul aanvullende dieet laer as die gewenste digtheid.

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Nutriënt status het gewys dat 36,4% van die babas anemies was, 16,1% van die babas het ’n ystertekort getoon (plasma ferritien konsentrasie < 12 12 µg/l) en 9,3% van die babas het aan ystertekort-anemie gely. Die antropometriese data het getoon dat 29,3% van die babas vertraagde groei gehad het (LAZ < 2) en 10,1% oorgewig was (WLZ > 2).

Ten opsigte van anemie-status, het manlike babas (OR= 1,388, p= 0,037) ’n groter kans getoon om anemies te wees. Babas vir wie uitsluitlike borsvoeding op die ouderdom van 0–2 maande gestaak is (OR= 0,620, p= 0,039;) en babas wat gereeld formule-melk ingeneem het (OR= 0,523, p= 0,001), het ’n laer risiko vir anemie getoon. Ten opsigte van ystertekort-status, het manlike babas (OR= 2,432, p= 0,002) ’n groter kans getoon om ’n ystertekort te hê; terwyl babas met ’n hoër geboortegewig (OR= 0,417, p=0,005), babas vir wie uitsluitlike borsvoeding op die ouderdom van 0–2 maande gestaak is (OR= 0,362, p= 0,022) en babas wat gereeld formule-melk ingeneem het (OR= 0,219, p= 0,001), ’n laer kans getoon het om ’n ystertekort te hê.

Hemoglobienstatus het positief bygedra tot oog-hand-koördinasie, lokomotoriese ontwikkeling en gekombineerde psigomotoriese ontwikkeling [β= 0.677 (0.343, 1.011), p= < 0.001)]; [β= 0.439 (0.164, 0.714), p= 0.002]; [β= 1.116 (0.586, 1.645), p= < 0.001], onderskeidelik. Gereelde verbruik van kommersiële babagraankos (≥4 dae per week) het ’n positiewe bydra gemaak tot die lokomotoriese ontwikkeling [β= 0.709 (0.043, 1.376); p= 0.037)] en ouer-graderingstellingstellings [β= 1.506 (0.912, 2.100); p= < 0.001]. Ekslusiewe borsvoeding vir die ouderdom van 0–2 maande teenoor die ouderdom van van 5–6 maande, het positief bygedra tot ouer-graderingstellings [β= 1.544 (0.673, 2.414), p = 0.001)]. Manlike geslag was geassosieeer met laer ouer-graderingstellingstellings [β= –0.673 (–1.256, –0.089), p = 0.024] teenoor vroulike geslag. Bevindinge vir die aanvaarbaarheidsproef het getoon dat, tydens Deel 1, meer as 70% van die moeders ’n telling van ≥4 vir sensoriese eienskappe by beide die klein-hoeveelheid lipied-gebaseerde voedingsaanvullings toegeken het. Hierdie resultaat dui aan dat beide aanvullings goed ontvang is. Vir Deel 2, was die gemiddelde verbruik vir aanvulling A en B wat vir die tydperk van twee weke aangemeld is, onderskeidelik 65,3±34,2% en 62,0±31,3% van die 20 g daaglikse porsie. Daar is tydens fokusgroepbesprekings ’n positiewe houding teenoor die aanvullings in die studiebevolking bevestig.

Gevolgtrekking

Hierdie studie het getoon dat voedingspraktyke tydens ‘n vroeë ouderdom, (borsvoedingspraktyke ingesluit) implikasies het op nutriënt status en/of ysterstatus wat psigomotoriese ontwikkeling beinvloed. Assosiasies wat gevind is tussen voedingspraktyke en psigomotoriese ontwikkeling kan deur die ysterstatus, wat deur voedingspraktyke beinvloed word, verduidelik word. Hierdie studie beklemtoon die belangrikheid van voldoende voeding en ysterstatus tydens n vroeë ouderdom van ontwikkeling.

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Sleutelterme: Baba, voedingspraktyke, voedingstatus, psigomotoriese ontwikkeling, aanvaarbaarheid, klein-hoeveelheid lipied-gebaseerde voedingsaanvullings

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ABBREVIATIONS

AA Arachidonic acid

AGP Alpha-1 glycoprotein

AI Adequate intake

AIDS Acquired immunodeficiency syndrome

ANC Antenatal care

APP Acute phase response proteins

BANC Basic antenatal care

BME Breast milk energy

BSID Bayley scales of infant development CDATs Child development assessment tools

CF Correction factors

CHW Community health workers

CI Confidence Interval

CTC Community therapeutic care

CRP High-sensitivity C-reactive protein

DHA Docosahexaenoic acid

DNA Deoxyribonucleic acid

DOH Department of Health

DPME Department of Performance, Monitoring and Evaluation DSD Department of Social Development

EAR Estimated average requirement

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EFA Essential fatty acids

ELISA Enzyme-linked immunosorbent assays

EPA Eicosapentaenoic acid

FAO Food and Agriculture Organization FBDG Food-based dietary guidelines

Fer Plasma ferritin

GMP Growth monitoring and promotion

HAZ Height-for-age z-score

HIV Human immunodeficiency virus

HSRC Human Sciences Research Council

ID Iron deficiency

IDA Iron deficiency anaemia

IFPRI International Food Policy Research Institute IMCI Integrated management of childhood illness

IQR Interquartile range

IYCF Infant and young child feeding KDI Kilifi developmental inventory

LC Long-chain

LCPUFAS Long-chain polyunsaturated fatty acids LNS Lipid-based nutritional supplements LNSs Lipid-based nutrient supplements MAM Moderate acute malnutrition MBFI Mother-baby friendly initiative

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iii MDGs Millennium development goals MMN Multiple micronutrient

MNP Micronutrient powders

MCTC Mother-to-child transmission MUAC Middle-upper-arm circumference MUFAs Mono-unsaturated fatty acids NFCS-FB-1 National Food Consumption Survey

PHC Public health care

pRBP Retinol-binding protein

pROH Plasma retinol

PUFAs Polyunsaturated fatty acids

RNA Ribonucleic acid

RUTF Ready-to-use therapeutic food SAM Severe acute malnutrition

SD Standard deviation

SDGs Sustainable development goals

SF Serum ferritin

SFAs Saturated fatty acids

SQ-LNS Small quantity lipid based nutritional supplements SUN Scaling up nutrition

TB Tuberculosis

TfR Transferrin receptor

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UIC Urine iodine concentration

UNICEF United Nations Children’s Fund

VAD Vitamin A deficiency

VAS Vitamin A supplementation

WHA World Health Assembly

WHO World Health Organization WHZ Weight-for-height z-score WLZ Weight-for-length z-score

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LIST OF TABLES

Chapter 1–2

Table 1 Research Team 6

Table 2 Criteria that define selected infant feeding practices (WHO 2008) 21 Table 3 Classification for assessing the severity of malnutrition by prevalence

ranges among children under 5 years of age (WHO, 2015b)

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Table 4 Age categories (months) (95% CI) for achievement for six gross motor milestones

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Table 5 Global progress of stunting, exclusive breastfeeding and wasting toward the global WHA targets

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Table 6 Comprehensive summary of key nutritional interventions in South Africa

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Chapter 3

Table 1 Socio-economic characteristics of the primary caregivers 106 Table 2 Feeding practices for 6 month old infants 107 Table 3 Amount of iron (mg) contribution from main reported food groups, for

consumers only

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Table 4 Nutrient density (per 100 kcal) of the complementary diet (excluding breast milk) and percentage of infants with an intake below desired density

109

Table 5 Anaemia-, iron- , CRP- and AGP and anthropometric status of infants 110 Table 6 Total nutrient intake for anaemic and non-anaemic infants (median,

IQR)

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Table 7 Comparison of anaemic and non-anaemic infants regards birth weight, gender, anthropometry and early feeding practices

112

Table 8 Bivariate relationships between anaemia and various potential associated factors

114

Table 9 Bivariate relationships between ID based on plasma ferritin and various potential associated factors

115

Table 10 Bivariate relationships between ID based on TfR and various potential associated factors

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ii Chapter 4:

Table 1 Nutritional status of 6-month-old infants and scores (mean, 95% CI) obtained in psychomotor development- and parent rating activities

136

Table 2 Comparison between development scores and caregiver's level of education, gender, early feeding practices, frequently consumed food items, anaemic- and iron status, growth status and birth weight of 6-month-old infants (mean, 95% CI)

137

Table 3 Multivariate linear regression analysis for psychomotor development 139 Table 4 Multivariate linear regression analysis for parent rating scores 140 Chapter 5:

Table 1 Nutrient content of the two SQ-LNS pastes 160 Table 2 Characteristics of the participants for Part 1 and Part 2 of the study 162 Table 3 Hedonic scores reported by the mother on her practical experience of

using the two porridge-SQ-LNS-mixtures in Part 1 of the study

163

Table 4 Frequencies of the mother’s own acceptance and perception of infant acceptance of the SQ-LNS-pastes after two weeks of home-use (Part 2 of the study) expressed as percentage

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LIST OF FIGURES

Chapter 2:

Figure 1 Global summary of some nutrition indicators for children younger than 2 years

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Figure 2 Breastfeeding practices in South Africa in relation to Eastern and Southern Africa and the world

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Figure 3 Prevalence of anaemia and vitamin A deficiencies in children younger than 5 years globally

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Figure 4 Global prevalence of underweight, stunting, wasting and overweight for children younger than 5 years

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Figure 5 The prevalence of stunting, wasting and underweight in children younger than 5 years at national and provincial level (below -2 SD)

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Figure 6 Prevalence of underweight, stunting and wasting in the world, Eastern and Southern Africa and South Africa

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Figure 7 Actions needed to achieve optimum infant and child nutrition and development

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Chapter 5

Figure 1 Representation of the research approach used for Part 1 165 Figure 2 Representation of the research approach used for Part 2. 166 Figure 3 Time used to consume SQ-LNS A and –B and control porridge

respectively

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Figure 4 Percentage of mothers who reported ‘Agree’ on both her own liking and her perception of the infant’s liking of the two porridge-SQ-LNS-mixtures and the control porridge in Part 1 of the study; *The term ‘Agree’ refers to the combination of ‘agree’ and ‘tend to agree

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CHAPTER 1

1.1 Rationale of the study

Infants that are exclusively breastfed for the first 6 months of life have a fourteen times less chance to die than non-breastfed infants, and breastfed children in general have at least a 6 times greater chance for survival. Breastfeeding reduces the risk of major mortality risk factors such as acute respiratory infection and diarrhoea (Black et al., 2008). Exclusive breastfeeding for the first 6 months can reduce stunting by protecting the infant against gastrointestinal infections (Kramer & Kakuma, 2012). Almost all stunted growth take place in the first thousand days after conception and the prevalence of stunting during this period may indicate poorer cognitive and educational outcomes later in life (Black & Alderman et al., 2013). The first 6 months of life is important as it is part of the ‘brain growth spurt’ period (starting in the third trimester and lasting for the first few months of life) when nutrition has a particularly significant effect on brain development (Isaacs & Oates, 2008). Nutritional deficits during the first 2 years of life may cause long-term impairment in growth and intellectual performance (Prado & Dewey, 2014).

Globally, breastfeeding is poorly practiced. Only 44% of new-borns receive breast milk within 1 hour after birth and less than 40% of children under 6 months are fed only breast milk with no additional foods or liquids (including water) (IFPRI, 2014). Already in 2003, The Global Strategy for Infant and Young Child Feeding was developed by the World Health Organization and United Nations Children's Fund (UNICEF) to improve feeding practices globally (WHO & UNICEF, 2003). However, still, one of the World Health Assembly (WHA) nutrition targets is to increase exclusive breastfeeding by 50% in 2025 (IFPRI, 2014; UNICEF, 2014). The prevalence of exclusive breastfeeding in South Africa for infants younger than 6 months is very low (7.4%) (HSRC, 2013). Even though early initiation of breastfeeding is practiced by an estimated 60% of mothers and breastfeeding is a common practice in South Africa, mixed feeding rather than exclusive breastfeeding is practiced (HSRC, 2013). The estimated prevalence of breastfeeding up to 2 years is only 31% (UNICEF, 2014).

South Africa is a member of the United Nations and adopted the WHA International code of Marketing of Breast-milk Substitutes, which points to commitment to protect and promote breastfeeding in the country. The Tshwane Declaration for the Support of Breastfeeding (see Annexure 1, Box 1) was published in 2011 (DOH, 2013a) to call on stakeholders to mainstream breastfeeding in all relevant policies, legislation, strategies and protocols and to

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provide services to support mothers to exclusively breastfeed their infants for 6 months, to start with appropriate complementary feeding and continue breastfeeding for up to 2 years of age and beyond. Recent studies have indicated that the implementation of this declaration on national level is not yet optimal as the introduction of semi-solid maize-based foods and formula milk before the age of 4 months is a common feeding practice (Du Plessis, 2013; Faber et al., 2014; Goosen et al., 2014). Nutrition-related indicators from South African District Health Information Systems indicate a significant under-reporting of the exclusive breastfeeding rate at 6 months and of growth monitoring, making it difficult to identify priority areas where intervention is needed. In terms of food availability, there is also a lack of data on the dietary diversity of pregnant women and children younger than 5 years (DOH, DSD, DPME, 2014). In most low-income communities, the first semi-solid foods given to infants are cereal-based gruels with low energy and nutrient density and low bioavailable iron due to the presence of phytic acid (Dewey, 2013). Nutrient density impacts micronutrient status (Troesch, et al. 2015). Globally, iron deficiency (ID) is the most common nutritional deficiency and more than 30% of the prevalence of anaemia is due to iron deficiency (Benoist et al., 2008; WHO, 2015b). The risk of ID and anaemia is higher during infancy, which is a period of rapid growth and development where iron is an important component of the haemoglobin molecule and a key nutrient needed for neurodevelopmental processes of the brain during infancy (Tolentino & Friedman, 2007; Hermoso et al., 2011; Prado & Dewey, 2014). Another nutrient of public health significance is vitamin A. Vitamin A deficiency weakens the immune system and increases the risk for morbidity and mortality (WHO, 2013a). Research on feeding practices in the age group 0–6 months associated with key nutrients like iron and vitamin A is lacking in a South African context.

Poor nutrition and development in the first few years of life have serious public health implications and contribute to early age morbidity and mortality (Bentley et al., 2014). Currently, there is a strong focus on scaling up interventions to integrate nutrition and early development (Black & Dewey, 2014; Sabanathan et al., 2015). Presently, many organisations and companies have shown interest in the development of small-quantity lipid-based nutrient supplements (SQ-LNS) and in their potential use in a variety of cultural and geographical settings (Arimond et al., 2013). SQ-LNS is a type of home fortification and can contribute to energy, protein and essential fatty acids (EFA) needed for healthy development (Gibson, 2011; Arimond et al., 2013). Two new SQ-LNS were developed for potential use in the South African setting. Both SQ-LNS are made from soy, which is less expensive than peanuts and which contains essential fatty acids and micronutrients needed for infant development

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(Georgieff, 2007; Gibson, 2011). The effects of these 2 SQ-LNS on linear growth in infants enrolled at age 6 months and followed until age 12 months are currently being investigated in a randomised controlled trial, which is referred to as the Tswaka study (Tswaka meaning “mixing” in the Setswana language). The acceptance of SQ-LNS for infant feeding at a home use level is important to ensure large scale sustainable use. The acceptance of SQ-LNS has not yet been established in South Africa.

1.2 Aim and objectives 1.2.1 Aim

This study investigated the nutritional status, early feeding practices and psychomotor development of 6-month-old infants residing in the peri-urban Jouberton area in Klerksdorp in the North West province, South African. Since different home fortification products to improve nutrient intake for infants are being investigated, the acceptance of two novel SQ-LNS for complementary feeding by infants and their primary caregiver in the study community was determined.

1.2.2 Objectives

The objectives were the following:

1. Determine retrospectively infant feeding practices during the first 6 months of life by investigating the following,

a. Initiation, duration of and type of breastfeeding practice b. Occurrence and age of introduction of milk feeding

c. Age of introduction of solid-, semi-solid or soft foods and other liquids. 2. Determine dietary intake of infants at the age of 6 months.

3. Determine the iron status and prevalence of anaemia in infants at 6 months taking into account plasma ferritin, plasma transferrin receptor and haemoglobin.

4. Determine the association of feeding practices, iron status and anaemia of 6-month-old infants.

5. Determine the association of psychomotor development, feeding practices, anaemia, iron and anthropometric status at 6 months.

6. Determine the acceptance of 2 novel SQ-LNS for complementary feeding by infants and their primary caregiver.

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4 1.3 Study site and design

This study is embedded within a randomised controlled efficacy trial, the Tswaka study, which was designed to investigate the effects of two newly developed SQ-LNS on linear growth and motor development. The Tswaka study was done in the peri-urban Jouberton area in the greater Matlosana Municipality in Klerksdorp, South Africa. The study site is 200 km from the nearest metropolitan area (Johannesburg).

This study was done in 2 phases:

Phase 1: An acceptability trial to determine the acceptability of the two novel SQ-LNS preceded the randomised control trial. The acceptability trial consisted of a sensory evaluation part with a cross-over design, followed by a two-week home use trial and focus group discussions to provide information on practicality of use in the home environment.

Phase 2: A cross-sectional study used the baseline data of the Tswaka study involving 750, 6-month-old infants.

1.4 Structure

The structure of this thesis is in article format and it is divided into 6 chapters. The format and referencing style of the 3 articles (Chapters 3 – 5) are according to the respective journals’ guidelines and these are indicated at the start of each relevant chapter.

Chapter 1 provides the background information, aim and objectives, structure of the thesis and information about the research team.

Chapter 2 summarises the relevant literature on infant and child feeding practices, key micronutrient deficiencies, motor development and strategies to improve infant and child feeding.

Chapter 3 presents the first article manuscript. The title of Manuscript 1 reads 'Feeding practices in relation to nutritional status of 6-month old infants from a peri-urban setting in South Africa.' This manuscript documents early infant feeding practices in relation to anaemia, iron status and anthropometric measurements at 6 months in infants in a peri-urban South African community. This manuscript will be submitted to Maternal and Child Nutrition. A content and style guideline for Maternal and Child Nutrition is presented in Annexure 2 and is also applicable for Manuscript 2.

Chapter 4 presents the second article manuscript. The title of manuscript 2 is ‘The association of psychomotor development with feeding practices and nutritional status

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of 6-month-old infants in a peri-urban community of South Africa'. In this manuscript the association of psychomotor development regards feeding practices and nutritional status of 6-month-old infants are investigated. Manuscript 2 will be submitted to Maternal and Child Nutrition.

Chapter 5 presents the third article manuscript. The title of manuscript 3 is 'Acceptability of novel small quantity lipid-based nutrient supplements for complementary feeding in a peri-urban South African community.' This manuscript documents the research that determined the acceptability of two newly developed SQ-LNS pastes in a peri-urban South African community. This article has been published in the Food and Nutrition Bulletin (doi: 10.1177/0379572115616057). A content and style guideline for Food and Nutrition Bulletin is presented in Annexure 3. The published version of this manuscript can be found in Annexure 4.

Chapter 6 comprises a conclusion that summarises the essential findings of the study and provides recommendations.

1.5 Research team

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Table 1. Research Team

Members of the research team

Role

Prof. Marius Smuts Co-promoter of PhD thesis. Principal Investigator of Tswaka trial. Overall responsibility for design and execution of Tswaka trial; quality control of laboratory analysis.

Guidance regarding writing of dissertation and interpretation of results. Co-author of all manuscripts.

Prof. Mieke Faber Co-promoter of PhD thesis. Co-Principal Investigator of Tswaka trial. Questionnaire development, fieldforker training, data coding and analysis for dietary data.

Guidance regarding writing of dissertation and interpretation of results. Co-author of all manuscripts.

Dr. Namukolo Covic Promoter of PhD thesis. Guidance regarding protocol development for of acceptability trial. Questionnaire development and fieldworker training for psychomotor assessment.

Guidance regarding writing of dissertation and interpretation of results. Co-author of all manuscripts

Marinel Rothman Ph.D. student. Protocol development, execution and data management of the acceptability trial. One of the study

coordinators of the Tswaka randomized controlled trial. Involved in questionnaire development and fieldworker training for the Tswaka trial. Supervision of data collection and quality control of dietary data, feeding practices and psycho-motor development. Data analysis for acceptability study and (in consultation with M Cockeran) for cross sectional data. Interpretation of results. Leading author on all manuscripts.

Prof. Salome Kruger Provided training on anthropometric measurements and analysis; standardization of anthropometry measurement.

Prof. Jane Kvalsvig Psychologist who provided guidance on psychomotor testing. Marike Cockeran Statistician who provided guidance regarding statistical analysis for

manuscripts.

Elleanor Rossouw Coordination and management of laboratory procedures Sr. Chrissie Lessing Registered Nursing sister: Overall responsible for clinical

procedures and blood sample collection.

Tonderayi Matsungo One of the study coordinators of Tswaka trial. Supervision of data collection and quality control of anthropometric data. Co-author on 2 manuscripts.

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7 1.6 References

Arimond, M., Zeilani, M., Jungjohann, S., Brown, K.H., Ashorn, P., Allen, L.H., Dewey, K.G., 2013. Considerations in developing lipid‐based nutrient supplements for prevention of undernutrition: experience from the International Lipid‐Based Nutrient Supplements (iLiNS) Project. Maternal and child nutrition, May 6. doi: 10.1111/mcn.12049.

Benoist, B.D., McLean, E., Egll, I. & Cogswell, M. 2008. Worldwide prevalence of anaemia 1993-2005: WHO global database on anaemia. Geneva: World Health Organization.

Bentley, M.E., Johnson, S.L., Wasser, H., Creed‐Kanashiro, H., Shroff, M., Fernandez Rao, S., et al. 2014. Formative research methods for designing culturally appropriate, integrated child nutrition and development interventions: an overview. Annals of the New York academy of sciences, 1308(1):54-67.

Black, M.M. & Dewey, K.G. 2014. Promoting equity through integrated early child development and nutrition interventions. Annals of the New York academy of sciences, 1308(1):1-10. Black, R.E., Allen, L.H., Bhutta, Z.A., Caulfield, L.E., De Onis, M., Ezzati, M., et al. 2008. Maternal and child undernutrition: global and regional exposures and health consequences. The lancet, 371(9608):243-260.

Black, R.E., Alderman, H., Bhutta, Z.A., Gillespie, S., Haddad, L., Horton, S., et al. 2013. Maternal and child nutrition: building momentum for impact. The lancet, 382(9890):372-375. Black, R.E., Victora, C.G., Walker, S.P., Bhutta, Z.A., Christian, P., De Onis, M., et al. 2013. Maternal and child undernutrition and overweight in low-income and middle-income countries. The lancet, 382(9890):427-451.

Dewey, K.G. 2013. The challenge of meeting nutrient needs of infants and young children during the period of complementary feeding: an evolutionary perspective. The journal of nutrition, 143(12):2050-2054.

DOH (Department of health) see South Africa.

Du Plessis, L.M. 2013. Commitment and capacity for the support of breastfeeding in South Africa: a paediatric food-based dietary guideline. South African journal of clinical nutrition, 26(3):S120-S128.

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Faber, M., Laubscher, R. & Berti, C. 2014. Poor dietary diversity and low nutrient density of the complementary diet for 6‐ to 24‐month‐old children in urban and rural KwaZulu‐Natal, South Africa. Maternal and child nutrition,doi: 10.1111/mcn.12146. Date of access: 19 Aug. 2014.

Georgieff, M.K. 2007. Nutrition and the developing brain: nutrient priorities and measurement. The American journal of clinical nutrition, 85(2):614S-620S.

Gibson, R. 2011. Strategies for preventing multi-micronutrient deficiencies: a review of experiences with food-based approaches in developing countries. In: Thompson, B., & Amoroso, L., (eds). Combating micronutrient deficiencies: food-based approach. CABI and FAO, Oxfordshire: UK:1-92.

Goosen, C., McLachlan, M. & Schübl, C. 2014. Infant feeding practices during the first 6 months of life in a low-income area of the Western Cape Province. South African journal of child health, 8(2):50-54.

Hermoso, M., Vollhardt, C., Bergmann, K. & Koletzko, B. 2011. Critical micronutrients in pregnancy, lactation, and infancy: considerations on vitamin D, folic acid, and iron, and priorities for future research. Annals of nutrition and metabolism, 59(1):5-9.

HSRC (Human Sciences Research Council). 2013. The South African National Health and Nutrition Examination Survey (SANHANES-1). Data analysis on infant feeding practices, and anthropometry in children under five years of age: South Africa 2012. Report for UNICEF. Cape Town.

IFPRI (International Food Policy Research Institute). 2014. Global nutrition report 2014: actions and accountability to accelerate the world's progress on nutrition. Washington, DC. Isaacs, E. & Oates, J. 2008. Nutrition and cognition: assessing cognitive abilities in children and young people. European journal of nutrition, 47(3):4-24.

Kramer, M.S. & Kakuma, R. 2012. Optimal duration of exclusive breastfeeding. Cochrane database dystematic review, 8:1-131.

Prado, E.L. & Dewey, K.G. 2014. Nutrition and brain development in early life. Nutrition reviews, 72(4):267-284.

Sabanathan, S., Wills, B. & Gladstone, M. 2015. Child development assessment tools in low-income and middle-low-income countries: How can we use them more appropriately? Archives of disease in childhood, 100:482-488.

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South Africa. Department of Health. 2013a. South African infant and young child feeding policy. Pretoria.

South Africa. Department of Health. 2013b. Roadmap for nutrition in South Africa 2013-2017. Pretoria.

Tolentino, K. & Friedman, J.F. 2007. An update on anaemia in less developed countries. The American journal of tropical medicine and hygiene, 77(1):44-51.

Troesch, B., Biesalski, H.K., Bos, R., Buskens, E., Calder, P., Saris, W.H.M. 2015. Increased of foods with high nutrient density can help break the intergenerational cycle of malnutrition and obesity. Nutrients, 7(7):6016-6037.

UNICEF (United Nations Children's Fund- Division of communication). 2014. Statistical tables: economic and social statistics on the countries and areas of the world, with particular reference to children's well-being. New York, USA.

WHO (World Health Organization). 2013. Essential nutrition actions: Improving maternal, new-born, infant and young child health and nutrition. Geneva, Switzerland.

WHO (World Health Organization). 2014. Maternal, infant and young child nutrition in East and Southern African countries: moving to national implementation. Report of a World Health Organization workshop, Entebbe, Uganda, 26–28 November 2013.

WHO (World Health Organization). 2015. Micronutrient deficiencies: iron deficiency anaemia. http://www.who.int/nutrition/topics/ida/en/ Date of access: 2 July 2015.

WHO & UNICEF (World Health Organization United Nations Children's Fund). 2003. Global strategy for infant and young child feeding. Geneva, Switzerland: World Health Organization.

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10

CHAPTER 2

Literature review on feeding practices, key selected micronutrient deficiencies, growth and development of infants and young children

Malnutrition, including undernutrition and micronutrient deficiencies, causes stunting and wasting, which are major risk factors for neonatal disorders, pneumonia and diarrhoea. These diseases cause the death of nearly eight million children each year (Bentley et al., 2014). Undernutrition can be reduced by improving exclusive breastfeeding practices and establishing optimal complementary feeding practices that include continuing breastfeeding for up to 2 years or beyond. This could save the lives of 1.5 million children younger than 5 years annually (WHO, 2013a).

This literature review firstly focuses on the importance of breastfeeding as a cornerstone for healthy growth and development. Secondly, optimal complementary feeding practices are discussed, followed by current international and national breastfeeding and complementary feeding practices. Against the background of current breastfeeding and complementary feeding practices, undernutrition in terms of micronutrient malnutrition, growth and development is discussed. Finally, some general actions needed to achieve optimum infant and child nutrition and development are reported.

2.1 Importance of breastfeeding

The 2003 Lancet series on child survival highlighted breastfeeding as the most important preventative approach for saving child lives (Jones et al., 2003). Breast milk is the best food source for optimal nutrient intake and it provides immunological protection. Breastfeeding has different benefits for both the mother and infant, including reducing the risk of major mortality risk factors like acute respiratory infection and diarrhoea (Black et al., 2008; Kramer & Kakuma, 2012).

The WHO recommends initiation of breastfeeding within the first hour after birth, exclusive breastfeeding until 6 months of age, and introduction of complementary foods at age 6 months with continued breastfeeding until the age of 2 years or older (WHO & UNICEF, 2014). The South African paediatric Food-based Dietary Guidelines Working Group formulated key messages with regard to infants younger than 6 months to be tested in a field setting. These messages are: 1) “give your baby only breast milk for the first 6 months. No other food or drink is needed at this age. If a baby is given other food and drink, he or she will consume less breast milk, and thereby receive less nutrition. Babies are protected against infection when

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they are breastfed; 2) hold your baby against your chest, skin-to-skin, within one hour of birth. Start breastfeeding at this time; 3) feed your baby several times during the day and night. This will help your body to make more milk; 4) breast milk contains substances that help to protect your baby against illness. If your baby does not get breast milk, he or she is at a greater risk of developing serious illnesses; 5) ask for help if your baby is having difficulty breastfeeding” (Du Plessis, 2013). A systematic review of evidence for breastfeeding initiation practices and neonatal outcomes has indicated that early initiation of breastfeeding (within one hour) decreased the risk of mortality by 44% (Debes et al., 2013). Initiation of breastfeeding within one hour after birth stimulates the production of breast milk from the mother and protects the infant from infection. The colostrum is an important source of nutrition and immune protection of the infant. Colostrum is special milk rich in white cells and antibodies, protein, minerals and fat-soluble vitamins A, D, E and K. The yellowish colour of colostrum is due to the presence of vitamin A. It also provides important immune protection for the infant’s first exposure to the micro-organisms in the environment. On the third day after delivery, the intake of breast milk increases to 300–400 ml per 24 hours, and then on the fifth day to 500–800 ml. Transitional milk is known as the kind of milk secreted from day 7–14 and the kind of milk secreted after 2 weeks is called mature milk (WHO, 2009b). Emotional bonding occurs between the infant and mother during breastfeeding. Early skin-to-skin care in neonates showed to increase the breastfeeding rate by 27% of infants aged 1–4 months and also has the potential to increase the duration of breastfeeding (Moore et al., 2012). Results of a systematic review showed that exclusive breastfeeding for the first 6 months, in comparison to exclusive breastfeeding for 3– 4 months, reduces gastrointestinal infection, increases maternal weight loss and has no adverse effect on growth. A reduced level of iron was observed, but delayed cord clamping and maternal iron supplementation can treat and rectify the situation (Kramer & Kakuma, 2012).

Breastfed infants are less likely to become overweight. A systematic review done by Horta and Victora (2013) showed that a longer duration of breastfeeding in children may reduce the prevalence of overweight or obesity later in life, and has a protective effect against type-2 diabetes (Horta & Victora, 2013). Breastfeeding was also shown to be associated with an increased intelligence in childhood and adolescence. All of the above findings must take residual confounding factors into consideration as breastfeeding duration was higher in more educated mothers with a higher income (Horta & Victora, 2013). A study conducted in the Honduras in different communities on poor income, less educated mother-infant pairs also

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showed that exclusively breastfed infants crawled sooner than those who were mixed-fed (Dewey et al., 2001).

In developing countries, bottle-fed infants are at a greater risk of illness, especially when considering diarrhoeal infections and pneumonia (Bahl et al., 2005) as the utensils used to prepare bottle feeding may be dirty and contaminated (Lanigan et al., 2001). An infant fed with an artificial teat may also have difficulties to learn to attach well at the breast, and feeding with an artificial teat has been associated with early cessation of breastfeeding (WHO, 2009b). 2.1.1 Nutrient content of breast milk

The nutrient content of breast milk is highly variable between individuals (Gidrewics et al., 2014) and derives from 3 sources: 1) the synthesis in the lactocyte; 2) dietary in origin, and 3) the maternal stores, which are especially important for fatty acid composition. The macronutrient composition of breast milk varies within mothers and across populations. The mean macronutrient composition is estimated to be 3.2–3.6 g/dl for fat, 6.7–7.8 g/dl for lactose and 0.9–1.2 g/dl for protein. The energy content is highly correlated with the fat content of breast milk and ranges from 65–70 kcal/dl (Ballard & Morrow, 2013). Unless the mother is deficient, breast milk is a sufficient source of most vitamins and minerals needed by the infant (WHO, 2009b). The composition of breast milk is discussed in short below.

Fat: An estimated 50% of energy in breast milk is provided by fats (German & Dillard, 2006). Brenna et al. (2007) reported from a descriptive meta-analysis that the mean concentrations of long-chain polyunsaturated fatty acids (LCPUFAs), namely docosahexaenoic acid (DHA) and arachidonic acid (AA) in breast milk are 0.32±0.22% and 0.47±0.13% respectively. These fats are both important for neural development (Brenna et al., 2007). The average breast milk intake of 750 ml for the first 6 months after birth seems to correspond with these concentrations (Cunnane et al., 2000). There is a higher concentration of DHA found in breast milk when compared to formula milk (Heaton et al., 2013). However, the availability of these LCPUFAs depend on the LCPUFAs stores at birth, available LCPUFAs from the diet and the ability of the infant to synthesize LCPUFAs from their shorter-chain precursors (Innis, 1991). Low-birth-weight preterm infants have limited stores of the LCPUFAS needed for rapid development at birth, and they need preformed dietary LCPUFAs (Innis, 2003; Larque et al., 2002). Maternal LCPUFA body stores are closely related to the LCPUFA content in breast milk (Del Prado, 2001). Mothers of preterm infants transfer less LCPUFAs to the foetus during the shorter pregnancy and provide a smaller volume of human milk for preterm infants and therefore might have higher LCPUFA stores than mothers of full-term infants (Kovács et al., 2005). Therefore,

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preterm infants need their own mother's milk, which might have a higher LPUFA content (Bokor et al., 2007).

Lactose: Milk sugar lactose is the main carbohydrate in breast milk and breast milk contains about 7 g lactose per 100 ml. Oligosaccharides present in breast milk provide important protection against infection (WHO, 2009b).

Protein: Many proteins in breast milk are digested and a good source of well-balanced amino acids. Breast milk contains adequate amounts of essential amino acids for the developing infant. Lipase, amylase, β-casein, lactoferrin, haptocorrin, helps in the digestion and utilisation of macro- and micronutrients from breast milk (Lönnerdal, 2003). The proteins in breast milk have many protective factors against infection, including immunoglobulin, which covers the intestinal mucosa and prevents the entry of bacteria into the cells; white blood cells, which protect against micro-organisms; and whey proteins, which protect against bacteria, viruses and fungi (WHO, 2009b).

Calcium: About half of the calcium found in breast milk is bound to proteins. Infants need a small amount of calcium for bone mineralisation because of the slow growth rate over a 3-month-period (Kent et al., 2009).

Choline: Breast milk is rich in highly bioavailable choline needed for cognitive development (Ilcol et al., 2005).

Vitamin A: Breast milk is an important source of vitamin A, which is needed by new-born infants with low liver vitamin A stores (Engle-Stone et al., 2014).

Iron and zinc: Iron and zinc are present in breast milk in low concentrations, but both are highly bioavailable (WHO, 2009b). During the third trimester of pregnancy, the term infant accretes 80% of iron. Iron requirements during the first 6 months of infancy are dependent on the iron stores at birth and infants born prematurely are deficient in total body iron (Baker & Greer, 2010). Maternal iron status (before and during pregnancy), gestational age, birth weight and the timing of the umbilical cord clamping all influence the iron status of the new-born infant at birth. A breastfed infant with a normal birth weight born from a mother with an adequate iron status during pregnancy and who experienced delayed umbilical cord clamping, will have sufficient iron for the first 6 months (Chaparro et al., 2006; Dewey & Chaparro, 2007; Hutton & Hassan, 2007).

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14 2.1.2 Other components and factors

Breast milk also contains a variety of bioactive components with medicinal qualities. Factors like growth factors (epidermal-, neuronal-, insulin-like-, vascular endothelial- and erythropoietin growth factors), growth-regulating hormones and immunological factors for the protection against infection and inflammation can also be found in breast milk (Ballard & Morrow, 2013).

2.2 Optimal complementary feeding

Complementary feeding is defined by WHO (2003) as the process starting when breast milk alone is no longer sufficient to meet the nutritional requirements of infants and therefore other foods and liquids are needed along with breast milk (WHO, 2003). During the introduction of complementary feeding, infants are particularly vulnerable and the nutrient adequacy of the diet is essential. The most challenging age group for meeting micronutrient needs falls within the second 6 months of life (Dewey, 2013). An adequately diverse diet that includes breast milk and a variety of plant and animal source foods is needed to provide approximately 40 different known nutrients in different amounts for optimal growth and development of the infant (Bloem, 2013). In developing countries, it is a challenge to feed nutrient dense complementary food to infants and young children in order to meet the nutritional requirements of especially iron, vitamin A, zinc, iodine and DHA (Black & Alderman et al., 2013; Black et al., 2008). These nutrients are discussed in more detail along with some key nutrients like choline, folate and vitamin B12 needed for optimal brain development (Prado & Dewey, 2014).

2.2.1 Selected key nutrients and their functions

Iron: Iron is essential for the functioning of many biochemical processes, which include electron transfer reactions, gene regulation, binding and transport of oxygen, as well as the regulation of cell growth and differentiation (Beard, 2001). Rapid growth along with increased haemoglobin needs occurs during infancy. Iron is an important component of the haemoglobin molecule and a key nutrient needed to transport oxygen to all organs in the body (Hermoso et al., 2011; Prado & Dewey, 2014). The extent to which iron is absorbed from the diet and used for normal body functions is known as the bioavailability of iron. There are 2 types of dietary iron, namely nonheme iron, which is present in both plant foods and animal tissues, and heme iron, which comes from haemoglobin and myoglobin in animal source foods. Heme iron is more bioavailable and may contribute to ≥40% of total absorbed iron, while nonheme iron is much less well absorbed than heme iron. Inhibitors of iron absorption include phytate in

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based foods (main inhibitor of iron absorption); polyphenols found in plant foods and beverages such as tea (restricts nonheme and heme iron absorption); and proteins such as milk proteins, eggs and albumin. Ascorbic acid is an enhancer of iron absorption (Hurrell & Egli, 2010). Good sources of heme iron are meat, poultry, fish and eggs (WHO, 2005). Vitamin A: Vitamin A is required in small amounts for the normal functioning of the visual systems, maintenance of cell function for growth, epithelial cellular integrity, immune function and reproduction (WHO, 2009a). Vitamin A is involved in the regulation of neurodevelopment by promoting cell differentiation and regulating the expression of genes and is also involved in dopamine-regulated cognitive and motor activity (Anjos et al., 2013). Dietary requirements for vitamin A are provided by a mixture of preformed vitamin A (retinol) present in animal source foods and provitamin A carotenoids, which are found in plant source foods and that need to be converted into retinol in the intestinal mucosa and the liver to be taken up by cells. Good sources of retinol include organ meat, dairy products, egg yolk, whereas β-carotene (pro-vitamin A) can be found in yellowish fruits and vegetables like papaya and pumpkin (WHO, 2009a).

Zinc: As the fourth most abundant ion in the brain; zinc contributes to brain structure and function through: 1) DNA and RNA synthesis; 2) the metabolism of macronutrients and 3) the synthesis of co-enzymes for biogenic-amine synthesis and metabolism (Sandstead et al., 2000). Zinc plays a central role in cellular growth, differentiation and metabolism (Brown, Wuehler et al,. 2001) and is vital for nucleic acid and protein synthesis, gastrointestinal and immune function for healthy growth (Moynahan, 1974; MacDonald, 2000). Sources of zinc include red meat, poultry and fortified cereals (WHO & FAO, 2006).

Iodine: Iodine is seen as the primary potentially preventative micronutrient in cognitive disabilities during childhood (Aburto et al., 2014). Iodine is used for the synthesis of thyroid hormones needed for the development of the central nervous system through neurogenesis, neuronal migration, axon and dendrite growth, synaptogenesis and myelination (Prado & Dewey, 2014). Iodine deficiency causes poor growth, poor cognitive development and low urinary iodine excretion and in severe cases, iodine deficiency may cause death. Iodine deficiency disorders include a spectrum of growth, developmental and functional abnormalities and the swelling of the thyroid gland is the most common manifestation of iodine deficiency. Severe iodine deficiency during pregnancy results in foetal death or cretinism, whereas mild and moderate deficiency during pregnancy causes poor foetal development and a high risk of

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speech and hearing defects, as well as impaired motor development and growth (Aburto et al., 2014). Iodine can be found in iodised salt and fortified cereals (WHO & FAO, 2006). Choline, folate and vitamin B12: Choline is critical during the period of growth and development and is interrelated with folate (Zeisel, 2006). During periods of rapid growth and cell division, especially during pregnancy, folate’s role for normal neural tube closure is well known and it is vital for brain development through nucleotide synthesis, methylation processes, DNA integrity and transcription (Hermoso et al., 2011; Anjos et al., 2013). Folate (vitamin B9) plays a central role in the synthesis and methylation of nucleotides needed for cell multiplication and tissue growth. Folate is closely interrelated to vitamin B12 and the combination of severe folate deficiency and vitamin B12 deficiency may cause megaloblastic anaemia (Aslinia et al., 2006). After 6 months of age, infants may be vulnerable to vitamin B12 deficiency if the breastfeeding mother is vitamin B12 deficient and/or the infant consumes a low amount of animal source food (Black, 2008). Choline, folate and vitamin B12 are found in animal source foods, legumes and dairy products (WHO & FAO, 2006).

Fats: Fats are the main source of energy for healthy growth and development during infancy. Key functions of fat with regard to the small stomach size of infants are that fat exhibit slow gastric emptying, prolong satiety, facilitate the absorption of lipid-soluble vitamins and provide EFAs (Uauy et al., 2000). Animal-derived foods, full-cream milk, avocados and spreads made from groundnuts, other nuts or seeds are good sources of fat (WHO, 2005)

Fatty acids: Dietary fatty acids are classified according to the degree of unsaturation namely: 1) saturated fatty acids (SFAs) with no double bonds; 2) mono-unsaturated fatty acids (MUFAs) with one double bond, and 3) long chain polyunsaturated fatty acids (LCPUFAs) with two or more double bonds in the carbon chain. Humans are unable to synthesise the essential polyunsaturated fatty acids (PUFAs) and must acquire it from their diet. LCPUFAs are subdivided into 12 families according to the location of double bonds, ranging from the n-1 to n-12 position countered from the terminal carbon of the fatty acid chain. The n-6 and n-3 family are the most important families in terms of human health and nutrition (FAO, 2010). The two most abundant LCPUFAs found in the brain are DHA and AA (Agostoni, 2008). Arachidonic acid (AA) is part of the n-6 PUFAs. Meat, eggs and fish are good sources of AA (FAO, 2010). Eicosapentaenoic acid (EPA) and DHA are part of the n-3 PUFAs and good sources of n-3 fatty acids are marine fish like mackerel, salmon, and sardine, as well as fish oils (FAO, 2010). LC PUFAs play an essential role in the developing brain where most of the PUFAs are concentrated. The development of the infant's brain lays the foundation for the structure of the

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adult's brain and therefore, the optimal intake of LPUFAs is very important. Studies indicated that there is strong evidence that n-3 fatty acids are essential for healthy development from the time in utero during pregnancy throughout life (Connor, 2000). Among LPUFAs, DHA plays the primary role in brain development from birth throughout infancy and is also concentrated in some retinal cells to support visual activity. DHA deficiencies may cause neurodevelopment deficits (McNamara & Carlson, 2006). It was found that DHA deficiency during brain growth may be related to neurological or neurodegenerative diseases later in life (Farquharson et al., 1995). Therefore, the intake of oily fish during pregnancy and breastfeeding is important for the developing foetus and infant (Heaton et al., 2013). AA and DHA are vital for the cerebral cortex during the last trimester of gestation and for the first 18 months of life, which is also known as the "growth spurt" of brain development when the developing brain is vulnerable to micronutrient deficiencies too (Nyaradi et al., 2013).

When comparing cognitive development in breastfed versus formula-fed infants, results of a meta-analysis showed that, after adjustment for appropriate key cofactors, breastfeeding was associated with significantly higher scores for cognitive development. The presence of long-chain polyunsaturated fatty acids (LPUFAs) in breast milk was given as possible reason for the higher cognitive scores in breastfed infants (Anderson et al., 1999).

2.2.2 Principles for complementary feeding

Children younger than 2 years have high nutrient needs to support growth and development. Therefore, complementary foods should be high in nutrient density as breast-fed infants consume relatively small amounts of foods in addition to breast milk (Dewey, 2013). The WHO published guiding principles for complementary feeding of both the breastfed and non-breastfed child (WHO, 2003; WHO, 2005). The principles are summarised in Table 1 in Annexure 1. These guidelines can be adapted to local feeding practices and conditions. Some of the most important terms with regard to optimal complementary feeding include energy and nutrient density and dietary diversity. Responsive feeding, good hygiene and proper food handling is also important in terms of how, when, where and by whom the child is fed (WHO, 2003).

Energy and nutrient density: For breastfed infants aged 6–8 months, the daily total energy required from the complementary diet depends on the breast milk energy (BME) intake, which varies from 552 kcal for low- to 160 kcal for high BME intake. From the age of 9 to 23 months, energy requirements from the complementary diet increase from 701 kcal to 1028 kcal for low BME intake, and from 257 kcal to 516 kcal for high BME intake (Dewey & Brown, 2003). During

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the first 6 months of life, dietary total fat should contribute 40–60% of energy (%E) for healthy growth and, depending on the physical activity of the child, and estimated 35% for age 6–24 months (FAO, 2010). The energy density of the available local foods guides the number of meals required for the non-breastfed child and is calculated from the energy requirements (by assuming a gastric capacity of 30 g/kg body weight/day). Five to six meals/day are needed to meet the energy requirements when energy density of foods is 0.6 kcal/g, 4 meals a day are needed when energy density is 0.8 kcal/g and 3 meals are needed when the energy density is 1.0 kcal/g (WHO, 2005).

Breastfed infants consume a small amount of complementary food in addition to breast milk. Complementary food should be high in nutrient density (amount of nutrient per 100 kcal of food). Iron and zinc are generally problematic nutrients (Dewey, 2013), because of the low concentrations in human milk. For infants in developing countries, the minimum target nutrient density for iron and zinc is 4.5 mg/100 kcal and 1.14 mg/100 kcal respectively at the age of 6–8 months (when assuming that the average energy need from complementary food is 200 kcal/d with an average intake of breast milk). The minimum iron and zinc densities of complementary foods are significantly lower in the second year of life (1.0 and 0.46 mg/100 kcal, respectively) (Dewey, 2013).

Dietary diversity: Daily dietary intake of at least four of seven food groups like 1) grains, roots and tuber; 2) legumes and nuts; 3) dairy products (milk yogurt, cheese), 4) flesh foods (meat, fish, poultry and liver/organ meats, 5) eggs, 6) vitamin A rich fruit and vegetables and 7) other fruits and vegetables is a good indication that the infant most probably consumed at least one animal source food and at least one fruit or vegetable with a staple food. Non-breastfed infants need a daily intake of approximately 200–400 ml of milk if adequate animal source foods are consumed, or 300-500 ml of milk if animal source foods are not consumed regularly. Milk sources include full-cream animal milk, Ultra High Temperature (UHT) milk, reconstituted evaporated (not condensed) milk, fermented milk or yoghurt and expressed milk (heat treated if mother is HIV-positive) (WHO, 2005).

Responsive feeding: Mothers or the primary caregiver are the main responsible persons to ensure the adequate nutrient intake for their infant or young child (IFPRI, 2014). Social interactions during feeding between caregivers and infants, like smiling and verbalisations, also promote the intake of food. Caregivers must be encouraged to participate in the development of the infant with simple activities such as play and communication, also during

Nutritional status, feeding practices and motor development of 6-month-old infants